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Am. J. Trop. Med. Hyg., 69(1), 2003, pp. 87-91
Copyright © 2003 by The American Society of Tropical Medicine and Hygiene

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LACK OF BASOPHILIA IN HUMAN PARASITIC INFECTIONS

EDWARD MITRE AND THOMAS B. NUTMAN
Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland


ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
While basophilia is often found in animal models of parasitic infection, it has not yet been established whether it occurs in parasite-infected humans. We investigated the relationship between basophilia and parasitic infections in humans by reviewing charts from 668 patients with confirmed parasitic infection (472 with only helminths, 146 with only protozoa, and 50 with both helminth and protozoan infections) and from 50 patients without parasitic infections. Basophilia (> 290 cells/mm3 ) occurred in only four of the 668 parasite-infected patients (0.6%), and there were no statistically significant differences in the percentages of patients with basophilia or in the absolute basophil counts among either the helminth-infected, protozoa-infected, or uninfected populations. Analysis with regard to relative basophil levels revealed that basophils constituted more than 3% of the peripheral white blood cell population in only four patients. Thus, basophilia occurs only rarely in human parasitic infections and is consequently not a useful clinical marker in the evaluation of suspected parasitic disease.


INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
It has long been known that basophilia occurs in animal models of parasitic infection. Two of the earliest reports of this phenomenon showed that bone marrow and circulating basophil counts increase within 48 hours following subcutaneous injection of ascaris body1 and ova fluid 2 into guinea pigs. Since then, several other investigators have reported similar findings in several different animal models of parasitic infection. Trichostrongylus colubriformis infection has been shown to increase basophil numbers in the bone marrow, small intestine, and peripheral circulation of guinea pigs.3 Infection of rats4–6 and gerbils7 with Nippostrongylus brasiliensis results in up to a 50-fold increase in peripheral basophil counts after two weeks. Trichinella spiralis infection in rats8 and guinea pigs9 also results in a marked basophilia that precedes the onset of eosinophilia by approximately one week. Fasciola infection of guinea pigs is associated with a chronic peripheral basophilia that is detectable up to four months after infection,10 and Strongyloides infection of Erythrocebus patas monkeys causes peripheral basophilia that is occasionally detectable for more than a month after infection.11

The presence of peripheral basophilia in human parasitic infections has not been as clear. While basophilia is mentioned as occurring in human parasitic infections in immunology and parasitology book chapters and review articles, the majority of investigators, with the exception of one reference to a doctoral thesis reporting peripheral basophilia in humans infected with Necator americanus,12 refer to other review articles,13 cite unpublished results,14 or provide no references for this finding.15–17

Because of the frequent finding of basophilia in parasitic infections of animals and the many allusions in the parasitologic and immunologic literature to such a phenomenon in humans, this study was conducted to determine whether peripheral basophilia is common in human parasitic infections.


MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Chart review. All available records of patients referred to the Clinical Parasitology Unit, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH) (Bethesda, MD) from 1979 to 2002 were manually reviewed by one investigator (E.M.). Almost all patients were referred from either a physician or a medical organization for evaluation of a possible parasitic infection or for entry into one of many ongoing NIAID clinical research protocols, each of which had been approved by the NIAID Institutional Review Board.

The following information was collected on every patient that met entry criteria: age, sex, parasitic diagnoses, complete white blood cell count with a differential count, IgE level (when available), and probable region of acquisition. Patients were classified as having acquired their parasitic infection as a consequence of being an immigrant to the United States, having visited friends and family abroad (VFF), or having been a traveler or temporary resident of a foreign country (expatriate). American patients whose source of exposure was the United States were classified in the expatriate category. The presence of basophilia was then evaluated in the following groups: all patients with helminths (AH), patients with only helminths (OH), patients with both helminth and protozoan infections (HP), and patients with only protozoan infections (OP). Additionally, data were collected on 50 subjects who were referred for possible parasitic infection (often because of eosinophilia), but whose evaluations failed to document a parasitic infection for use as a comparison group (U).

Inclusion/exclusion criteria. Criteria for inclusion included parasitic infection diagnosed at NIH and the existence of a complete blood count with a differential count done at NIH before antiparasitic treatment was initiated. Exclusion criteria included acquired immunodeficiency syndrome (AIDS), malignancy, ongoing systemic immunosuppression, primary hematologic disorder, or a history of antiparasitic (generally anthelmintic) therapy within two months prior to the first NIH visit.

Definition of parasitic infection. Parasitic infection was defined as either 1) positive identification of appropriate parasite stages on a stool examination, blood filtration, blood smear, urine sample, skin snip, or tissue biopsy; 2) positive result on a stool antigen-capture enzyme-linked immunosorbent assay for Giardia lamblia; 3) positive result in a polymerase chain reaction (PCR) for Loa loa in blood; 4) positive PCR result for Onchocerca volvulus in the skin; 5) positive circulating Wuchereria bancrofti antigen test result; 6) pathognomic magnetic resonance imaging findings or positive serology plus response to therapy for neurocysticercosis; 7) positive antifilarial serology plus Calabar swellings and response to therapy for L. loa; 8) positive antifilarial serology and either a Mazzoti reaction or ophthalmologic examination results consistent with onchocercal eye disease for O. volvulus; 9) positive serology and a consistent clinical picture for fascioliasis; or 10) meeting all the established criteria for tropical pulmonary eosinophilia.18 Not every patient underwent every investigation.

Basophil counts. Prior to 1980, all differential counts were performed by microscopic inspection of a peripheral blood smear. From 1980 to 1983, differentials were obtained using a Coulter Counter Model S PlusTM (Beckman-Coulter, Inc., Fullerton, CA) and confirmed by microscopy. From 1983 to 1995, differential counts were obtained only with the Coulter Counter Model S PlusTM. From 1995 until 2002, differentials counts have been measured via a Cell Dyn 3500TM or 4000TM (Abbott Laboratories, Abbott Park, IL).

The normal range for basophilia at the NIH (< 290 cells/ mm3) was established between 1980 and 1983 using data from 1,073 healthy volunteers (668 women and 405 men) and setting the upper limit for normal at the 97.5 percentile. Repeated tests with 100 healthy individuals upon switching to the Cell DynTM instrument in 1995 gave essentially identical results.

Statistical analysis. Comparisons of patient ages and absolute basophil counts were done using the nonparametric Mann-Whitney unpaired rank test. Comparisons of immigrant:expatriate ratios and of the percentages of patients with basophilia, eosinophilia, or elevated IgE levels were performed using Fisher’s exact test. All statistics were performed using StatView5 (SAS Institute, Cary, NC).


RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patients. Of the 1,346 cases reviewed, 728 (54%) had confirmed parasitic infections. Sixty of these were excluded for the following reasons: 48 did not have a complete blood count and differential count prior to therapy, 7 had taken anthelmintics in the preceding two months, 3 patients were receiving immunosuppressive therapy (all 3 had Strongyloides, 2 had also already received anthelmintic therapy), and 2 had AIDS (one had giardiasis and one had cryptosporidiosis).

The remaining 668 parasite patients plus 50 uninfected patients were included in the study. Of the patients with parasitic infections, 341 were expatriates (51.0%), 323 were immigrants (48.4%), and 4 were VFF (0.6%); 522 patients had at least one helminth infection. Of these, 472 were infected only with helminths and 50 were co-infected with protozoa. The remaining 146 patients were infected exclusively with protozoa.

The male:female ratio and the median ages were similar among the AH, OH, OP, and U groups (Table 1Go). The HP (mixed helminth/protozoa) group was significantly younger than each of the other groups (P < 0.01 for all comparisons). When stratified by demographic status, the HP group had a significantly greater number of immigrants compared to expatriates than the other groups (P < 0.03 for all comparisons). The AH and OH groups also had a greater immigrant: expatriate ratios than did the U patients and the OP group (P < 0.01 for all comparisons). There was no difference in the ratio of immigrants to expatriates between the OP and U groups (P = 0.46).


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TABLE 1
Characteristics of 668 parasite-infected and 50 uninfected patients evaluated by the National Institutes of Health Clinical Parasitology Unit*
 
Parasitic infections. The 668 parasite-infected patients harbored a total of 728 helminth and 208 protozoan infections; 481 patients had a single infection and the remaining 187 had infections with multiple parasites (range = 2–6, geometric mean = 2.4). Of the 661 parasite-infected patients in whom data on the region of acquisition were available, 317 had acquired their infection in Africa (48.0%), 227 in Asia (34.3%), 88 in Central and South America (13.3%), 23 in North America (3.5%), and 6 in Europe (0.9%).

Infections with filariae (138 with L. loa, 53 with O. volvulus, and 20 with W. bancrofti or tropical pulmonary eosinophilia), Strongyloides stercoralis (116), Leishmania species (100), and G. lamblia (70) were highly prevalent, likely reflecting the referral patterns to ongoing studies of these infections at NIH. Similarly, as a referral-only center our number of malaria cases was low. Hookworm infections were also very prevalent (n = 130). Each of the diagnosed parasitic infections and their probable region of acquisition are listed in Table 2Go.


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TABLE 2
Parasitic diagnoses and geographic regions of exposure of 668 parasite-infected and 50 uninfected patients*
 
Laboratory results. Basophilia (> 290 cells/mm3) occurred in only four of the 668 patients with documented parasitic infection: three patients with helminth infections and one with a protozoal infection (Table 3Go). These patients had hookworm alone, Mansonella perstans alone, a mixed infection with S. stercoralis and Hymenolepis nana, or cutaneous leishmaniasis. The absolute basophil counts (ABCs) in cells/mm3 and basophil percentages of the differentials for these patients were 483 (3%), 296 (2%), 292 (4%), and 400 (10%), respectively. There were no statistically significant differences in the numbers of patients with basophilia between any of the groups (P > 0.9 for all comparisons by Fisher’s exact test). There were also no statistically significant differences between any of the groups and the group without parasitic infection when comparing all the individual ABCs (P > 0.1 for all comparisons by the Mann-Whitney unpaired rank test).


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TABLE 3
Frequency of basophilia, eosinophilia, and elevated IgE levels in 668 parasite-infected and 50 uninfected patients
 
Analysis with regards to relative cell counts also did not show an increase in basophil levels because basophils constituted more than 3% of the peripheral white blood cell population in only four patients: the S. stercoralis/H. nana-infected and Leishmania patients mentioned earlier with basophil percentages of 4% and 10%, one S. mansoni-infected patient with 4% basophilia (ABC = 164), and one patient with a zoonotic filarial infection with 4% basophilia (ABC = 204). Only eight other patients had even 3% basophil levels in their white blood cell differential counts. Of note, other than their parasitic infections, all of the patients with either absolute or relative basophils were otherwise healthy, with no evidence of allergy, neoplasia, endocrinopathy, or myeloproliferative disease.

The percentages of patients with eosinophilia (67.6% in the AH group, 67.4% in the OH group, and 70% in the HP group) were significantly higher in all the groups of patients with helminth infection compared with the OP group (P < 0.0001 for all comparisons) and with the U patients (only 4% of patients with eosinophilia; P < 0.0001 for all comparisons).

When evaluated by individual parasite, hookworm and L. loa infections had the highest percentages of patients with eosinophilia (81.8% and 81.4%, respectively). Subjects with neurocysticercosis had the lowest incidence of eosinophilia (only 1 of 18 patients, 5.6%) among the helminth infections.

The IgE levels were also significantly elevated in those patients with helminth infections compared with the U patients: 77.5% of AH patients, 77.4% of OH patients, and 80% of HP patients had elevated IgE levels (defined as > 90 IU/ml) compared with 41.7% of the OP group (P < 0.001 for AH and OH and P = 0.17 for HP) and 30.8% of the U patients (P < 0.0001 for AH and OH and P = 0.06 for HP). The lack of statistical significance in comparing the HP group to the OP and U groups was likely due to the small number of HP patients with measured IgE levels (n = 5). There was no statistically significant difference between the percentages of patients with elevated IgE levels in the OP and U groups (P = 0.557).


DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Because of the many studies documenting the development of basophilia in experimental parasitic infections of animals1–11 and the frequent allusions in the literature to such a phenomenon in humans,12–17 we conducted a retrospective study to determine whether basophilia is a common finding in parasitic infections of humans. Of 668 patients with confirmed parasitic infection (472 with helminth infections, 146 with protozoan infections, and 50 with both helminth and protozoan infections), only 4 had an elevated peripheral basophil count. There were no statistically significant differences in either absolute or relative basophil counts among the populations with and without parasites.

While this finding clearly demonstrates that basophilia is not a useful clinical marker of parasitic disease, it does not exclude the possibility that basophils play an important role in helminth infections of humans. Indeed, a growing body of evidence suggests basophils are central to the human immune response to helminth infection.

Helminth infections, as reconfirmed in this study, are well known to be associated with high IgE levels.19–21 Basophils bind IgE through high-affinity receptors on their surface and degranulate and release histamine and other inflammatory mediators after cross-linking of these receptors.22 Basophils from Toxocara-, Ascaris-, Onchocerca-, Wuchereria-, Strongyloides-, and Schistosoma-infected patients have been shown to release histamine in response to parasite antigen.23–27 The amount of histamine released by basophils in response to Toxocara antigen was found to be proportional to the serum concentration of Toxocara antigen-specific IgE.23 In addition to high levels of IgE, human helminth infections are also associated with increased production of interleukin (IL)-4, the prototypical Th2 cytokine. Basophils from filaria-infected patients have been shown to release IL-4 in response to L3 larvae and filarial antigen,28 and basophils from uninfected individuals have been shown to release IL-4 after stimulation with Schistosoma egg antigen.29 Even though basophils make up only a small percentage of peripheral white blood cells, they have the ability to specifically recognize many different antigens by virtue of binding different IgE antibodies on their surface. Consequently, it is possible that the number of basophils that specifically recognize and are activated by helminth antigen may equal or even exceed the number of antigen-specific T cells responding to helminths. In asthmatic patients, basophils producing IL-4 have been shown to outnumber IL-4-producing T cells in response to dust mite antigen.30 Preliminary results using cells of filaria-infected patients show that the number of basophils producing IL-4 in response to filaria antigen is usually equal to or greater than the number of IL-4-producing CD4+ cells (Mitre E, unpublished data).

Basophils, by virtue of surface expression of CD40 ligand and production of IL-4, have the ability to induce B cells to isotype switch to IgE.31 Because basophils release IL-4 after cross-linking of receptor-bound IgE, production of which initially requires IL-4, basophils in helminth infections may serve to amplify an ongoing Th2 response.

Of interest, it has been demonstrated that a glycoprotein from S. mansoni eggs can cause basophils to degranulate and release IL-4 by binding and cross-linking non-antigen-specific IgE,29,32 raising the possibility that some helminth antigens may act as a type of "super allergen" by binding directly to the non-variable portion of IgE. This suggests that, in some cases, basophils may serve as the initial source of IL-4 that causes T cells to differentiate toward a Th2 phenotype in helminth infections.

Given the probable importance of basophils in the response to helminth infections, it is surprising that this study has shown that their numbers are not elevated in patients with helminth infections. One possible explanation for this apparent disconnection would be the existence of a mechanism for controlling basophil activity apart from fluxes in absolute numbers. In studies of basophils from patients receiving anti-IgE therapy, it has been shown that the number of IgE receptors on basophils can vary tremendously, from several thousand to well over 200,000 receptors per cell, and is proportional to the amount of IgE in the serum.33 Consequently, basophils may modulate their activity in response to helminth infection by increasing the number of high-affinity IgE receptors they have per cell rather than increasing their absolute cell numbers.

As expected, the percentages of patients with eosinophilia and elevated IgE levels found in this study were higher in the helminth groups than in the protozoan only and uninfected groups. The incidence of eosinophilia in parasite-infected patients is likely overestimated in our study because many of our patients are referred on the basis of an elevated eosinophil level. Indeed, the incidence of eosinophilia in helminth-infected patients in this study (67.6%) is substantially higher than the 41.5% reported in a recent analysis of eosinophilia in returned travelers to a tropical medicine clinic in Germany.34

In conclusion, we have shown that there is no association between helminth or protozoan infection and peripheral basophilia in humans and that, therefore, basophilia is not a helpful clinical marker in the evaluation of suspected parasitic disease. Basophils may still play an important role in the immune response to helminths, but that role does not include an increase in their total numbers.

Received January 21, 2003. Accepted for publication April 3, 2003.

Acknowledgments: We thank Daniel Hernandez for help in obtaining the medical records reviewed in this paper and Brenda Rae Marshall for help in the preparation of the manuscript.

Authors’ address: Edward Mitre and Thomas B. Nutman, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892.

Reprint requests: Thomas B. Nutman, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, 4 Center Drive, Room 4/126, National Institutes of Health, Bethesda, MD 20892, Telephone; 301-496-5398, Fax: 301-480-3757, E-mail: tnutman{at}niaid.nih.gov.


REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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